Structural hemispheric asymmetries in the human precentral gyrus hand representation

doi:10.1016/j.neuroscience.2012.02.044

Neuroscience

Volume 210, 17 May 2012, Pages 211-221

https://doi.org/10.1016/j.neuroscience.2012.02.044 Get rights and content

Abstract

The superior region of the precentral gyrus (preCG) is known to be actively involved with hand function and has been proposed as a possible neural correlate of handedness. To test this hypothesis, we used a combined voxel-based morphometric (VBM) asymmetry analysis of structural MRI, along with diffusion MRI (dMRI) tractography to investigate laterality indices of corticomotor white matter (WM) pathways, based on measures of fractional anisotropy (FA). The relationship between measures of motor performance and FA laterality indices was also investigated. In a cohort of 14 right-handed healthy participants, the VBM asymmetry analysis revealed an area within the preCG associated with hand representation. The tractography analysis revealed that this region possessed a number of major WM intrahemispheric connections to the brain stem, thalamus, cerebellum, postcentral, caudal middle and superior frontal, and superior and inferior parietal corticomotor regions. Within the corticospinal tracts, we found FA was significantly higher in the left hemisphere compared with the right. Furthermore, significant correlations were found between FA asymmetry measures projecting from this region, namely corticospinal tracts and those connecting the postcentral gyri, with grip strength and finger-tapping performance, respectively. A number of the motor pathways projecting from this region also exhibited leftward asymmetry of FA distributions. The findings from this study highlight the role of the left motor cortex in skilled motor performance and provide a framework for the study of the relationship between handedness and preCG hand representation in larger normative populations.

Highlights

▶VBM analysis of GM asymmetry identified precentral gyrus hand representation. ▶Corticospinal tract FA measures for the left hand representation were significantly elevated. ▶FA for the hand representation WM pathways correlated with hand motor performance. ▶Multiple hand representation pathways exhibited leftward intrahemispheric connectivity.

Section snippets

Participants

Fourteen healthy control participants were recruited into this study with a mean age of 54.6±12.7 years (range 33–72, 8 males). The participants were recruited as age-matched controls for an amyotrophic lateral sclerosis (ALS) study (Rose et al., 2012) and were subsequently invited to participate in this study. Based on the Waterloo Handedness Questionnaire (WHQ, Bryden, 1977), all participants were self-reported as being right handed (WHQ 29.6±7.5). None of the participants had specific hand

Results

Measures of hand performance for the various motor tasks are summarized in Table 1. As expected, our right-handed participants all performed significantly better with their preferred hand on all motor function tests. With regards to age-related effects, there were no significant correlations between any of the hand performance laterality indices and age. The correlation between age and FTT (r=0.58, P=0.03) was not significant after correction for multiple comparisons.

Discussion

This study highlights the potential of using dMRI and probabilistic tractography to identify key corticomotor preCG connections and relates asymmetrical patterns of connectivity with performance measures of hand function. Such an approach could be used to probe the neural correlates of handedness in large normative populations. Our analysis technique applied to a small cohort of normal right-handed participants revealed significant leftward asymmetry within a corticomotor region located within

Conclusion

In summary, we have shown significant leftward GM density asymmetry in right-handed normal participants within an area in preCG hand representation. Structural connectivity analysis revealed that this region had a number of major WM intrahemispheric connections to the brain stem, thalamus, cerebellum, postcentral, caudal middle and superior frontal, and superior and inferior parietal corticomotor regions. These corticomotor connections were generated in an automated fashion using a higher-order

Acknowledgments

The authors acknowledge the assistance of Maricel Roxas and Nicole Hutchinson in recruiting participants for this study and the Motor Neuron Disease Research Institute of Australia for their funding support.

References (74)

K. Amunts et al.
Interhemispheric asymmetry of the human motor cortex related to handedness and gender
Neuropsychologia
(2000)
S. Ardekani et al.
Exploratory voxel-based analysis of diffusion indices and hemispheric asymmetry in normal aging
Magn Reson Imaging
(2007)
J. Ashburner et al.
Voxel-based morphometry—the methods
Neuroimage
(2000)
S.G. Brown et al.
Preference and performance measures of handedness
Brain Cogn
(2004)
M.P. Bryden
Measuring handedness with questionnaires
Neuropsychologia
(1977)
R.S. Desikan et al.
An automated labelling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest
Neuroimage
(2006)
M. Dhamala et al.
Neural correlates of the complexity of rhythmic finger tapping
Neuroimage
(2003)
C.D. Good et al.
Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains
Neuroimage
(2001)
M. Guye et al.
Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo
Neuroimage
(2003)
G. Hammond
Correlates of human handedness in primary motor cortex: a review and hypothesis
Neurosci Biobehav Rev
(2002)

K. Amunts et al.

Postnatal development of interhemispheric asymmetry in the cytoarchitecture of human area 4

Anat Embryol (Berl)

(1997)

J. Andersson

Non-linear optimisation

Y. Bai et al.

Model-based registration to correct for motion between acquisitions in diffusion MR imaging

IEEE International Symposium on Biomedical Imaging: from Nano to Macro

(2008)

P.J. Basser et al.

Estimation of the effective self-diffusion tensor from the NMR spin echo

J Magn Reson B

(1994)

C. Beaulieu

The basis of anisotropic water diffusion in the nervous system—a technical review

NMR Biomed

(2002)

W. Boling et al.

Localization of hand motor activation in Broca's pli de passage moyen

J Neurosurg

(1999)

S.G. Brown et al.

Using hand performance measures to predict handedness

Laterality

(2006)

C. Büchel et al.

White matter asymmetry in the human brain: A diffusion tensor MRI study

Cereb Cortex

(2004)

D.V. Callaert et al.

Hemispheric asymmetries of motor versus nonmotor processes during (visuo)motor control

Hum Brain Mapp

(2011)

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Cognitive, Behavioral, and Systems NeuroscienceResearch PaperStructural hemispheric asymmetries in the human precentral gyrus hand representation

Abstract

Highlights

Section snippets

Participants

Results

Discussion

Conclusion

Acknowledgments

Neuropsychologia

Magn Reson Imaging

Neuroimage

Brain Cogn

Neuropsychologia

Neuroimage

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Neuroimage

Neurosci Biobehav Rev

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Med Image Anal

Neuroimage

Brain Res

Neurosurg Clin N Am

Magn Reson Imaging

Neuroimage

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Neuroimage

Neuroimage

Neuroimage

Neuroscience

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Neuroimage

Potential impact of a 32-channel receiving head coil technology on the results of a functional MRI paradigm

Clin Neuroradiol

Postnatal development of interhemispheric asymmetry in the cytoarchitecture of human area 4

Anat Embryol (Berl)

Non-linear optimisation

Model-based registration to correct for motion between acquisitions in diffusion MR imaging

IEEE International Symposium on Biomedical Imaging: from Nano to Macro

Estimation of the effective self-diffusion tensor from the NMR spin echo

J Magn Reson B

The basis of anisotropic water diffusion in the nervous system—a technical review

NMR Biomed

Localization of hand motor activation in Broca's pli de passage moyen

J Neurosurg

Using hand performance measures to predict handedness

Laterality

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Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Structural hemispheric asymmetries in the human precentral gyrus hand representation